Bioinformatics analysis of the locus for enterocyte effacement provides novel insights into type-III secretion

BMC Microbiology

Volumn 5, Issue , 2005, Pages

  Pallen, Mark J ^a   Beatson, Scott A ^a   Bailey, Christopher M ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; ESCHERICHIA COLI PROTEIN; ESCHERICHIA COLI SECRETED PROTEIN A; FLAGELLIN;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BIOINFORMATICS; CELL FUNCTION; GENE LOCUS; INTESTINE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; SEQUENCE HOMOLOGY; UNINDEXED SEQUENCE; YERSINIA;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; COMPUTATIONAL BIOLOGY; ENTEROCYTES; ESCHERICHIA COLI; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; YERSINIA ENTEROCOLITICA;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; YERSINIA;

EID: 18944390249     PISSN: 14712180     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-5-9     Document Type: Article

References (165)

1. Hueck CJ: Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 1998, 62:379-433.
2. Pallen MJ, Chaudhuri RR, Henderson IR: Genomic analysis of secretion systems. Curr Opin Microbiol 2003, 6:519-527.
3. Cornelis GR, Van Gijsegem F: Assembly and function of type III secretory systems. Annu Rev Microbiol 2000, 54:735-774.
4. Cornelis GR: Type III secretion: a bacterial device for close combat with cells of their eukaryotic host. Philos Trans R Soc Lond B Biol Sci 2000, 355:681-693.
5. Blocker A, Komoriya K, Aizawa S: Type III secretion systems and bacterial flagella: insights into their function from structural similarities. Proc Natl Acad Sci U S A 2003, 100:3027-3030.
6. Muller S, Feldman MF, Cornelis GR: The Type III secretion system of Gram-negative bacteria: a potential therapeutic target? Expert Opin Ther Targets 2001, 5:327-339.
7. Russmann H: Bacterial type III translocation: a unique mechanism for cytosolic display of heterologous antigens by attenuated Salmonella. Int J Med Microbiol 2003, 293:107-112.
8. Russmann H: Yersinia outer protein E, YopE. A versatile type III effector molecule for cytosolic targeting of heterologous antigens by attenuated Salmonella. Adv Exp Med Biol 2003, 529:407-413.
9. Kenny B: Mechanism of action of EPEC type III effector molecules. Int J Med Microbiol 2002, 291:469-477.
10. Kaper JB, Nataro JP, Mobley HLT: Pathogenic Escherichia coli. Nature Reviews Microbiology 2004, 2:123-140.
11. McDaniel TK, Jarvis KG, Donnenberg MS, Kaper JB: A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci U S A 1995, 92:1664-1668.
12. Jarvis KG, Giron JA, Jerse AE, McDaniel TK, Donnenberg MS, Kaper JB: Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. Proc Natl Acad Sci U S A 1995, 92:7996-8000.
13. McDaniel TK, Kaper JB: A cloned pathogenicity island from enteropathogenic Escherichia coli confers the attaching and effacing phenotype on E. coli K-12. Mol Microbiol 1997, 23:399-407.
14. Jerse AE, Yu J, Tall BD, Kaper JB: A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc Natl Acad Sci U S A 1990, 87:7839-7843.
15. Hacker J, Kaper JB: Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol 2000, 54:641-679.
16. Perna NT, Mayhew GF, Posfai G, Elliott S, Donnenberg MS, Kaper JB, Blattner FR: Molecular evolution of a pathogenicity island from enterohemorrhagic Escherichia coli O157:H7. Infect Immun 1998, 66:3810-3817.
17. Schauer DB, Falkow S: Attaching and effacing locus of a Citrobacter freundii biotype that causes transmissible murine colonic hyperplasia. Infect Immun 1993, 61:2486-2492.
18. Huys G, Cnockaert M, Janda JM, Swings J: Escherichia albertii sp. nov., a diarrhoeagenic species isolated from stool specimens of Bangladeshi children. Int J Syst Evol Microbiol 2003, 53:807-810.
19. Janda JM, Abbott SL, Albert MJ: Prototypal diarrheagenic strains of Hafnia alvei are actually members of the genus Escherichia. J Clin Microbiol 1999, 37:2399-2401.
20. Albert MJ, Faruque SM, Ansaruzzaman M, Islam MM, Haider K, Alam K, Kabir I, Robins-Browne R: Sharing of virulence-associated properties at the phenotypic and genetic levels between enteropathogenic Escherichia coli and Hafnia alvei. J Med Microbiol 1992, 37:310-314.
21. Webber C, Ponting CP: Genes and homology. Curr Biol 2004, 14:R332-3.
22. Pallen M: From Sequence to Consequence: In silico Hypothesis Generation and Testing. In Methods in Microbiology Volume 33. Edited by: Wren B and Dorrell N. London, Academic Press; 2002:27-48.
23. Pallen MJ, Beatson SA, Bailey CM: Bioinformatics, Genomics and Evolution of Non-Flagellar Type-III Secretion Systems: A Darwinian Perpective. FEMS Microbiol Rev 2005, 29:201-229.
24. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
25. Kenny B, Jepson M: Targeting of an enteropathogenic Escherichia coli (EPEC) effector protein to host mitochondria. Cell Microbiol 2000, 2:579-590.
26. McNamara BP, Donnenberg MS: A novel proline-rich protein, EspF, is secreted from enteropathogenic Escherichia coli via the type III export pathway. FEMS Microbiol Lett 1998, 166:71-78.
27. Elliott SJ, Krejany EO, Mellies JL, Robins-Browne RM, Sasakawa C, Kaper JB: EspG, a novel type III system-secreted protein from enteropathogenic Escherichia coli with similarities to VirA of Shigella flexneri. Infect Immun 2001, 69:4027-4033.
28. Tu X, Nisan I, Yona C, Hanski E, Rosenshine I: EspH, a new cytoskeleton-modulating effector of enterohaemorrhagic and enteropathogenic Escherichia coli. Mol Microbiol 2003, 47:595-606.
29. Neves BC, Mundy R, Petrovska L, Dougan G, Knutton S, Frankel G: CesD2 of enteropathogenic Escherichia coli is a second chaperone for the type III secretion translocator protein EspD. Infect Immun 2003, 71:2130-2141.
30. Elliott SJ, O'Connell CB, Koutsouris A, Brinkley C, Donnenberg MS, Hecht G, Kaper JB: A gene from the locus of enterocyte effacement that is required for enteropathogenic Escherichia coli to increase tight-junction permeability encodes a chaperone for EspF. Infect Immun 2002, 70:2271-2277.
31. Creasey EA, Friedberg D, Shaw RK, Umanski T, Knutton S, Rosenshine I, Frankel G: CesAB is an enteropathogenic Escherichia coli chaperone for the type-III translocator proteins EspA and EspB. Microbiology 2003, 149:3639-3647.
32. Mellies JL, Elliott SJ, Sperandio V, Donnenberg MS, Kaper JB: The Per regulon of enteropathogenic Escherichia coli : identification of a regulatory cascade and a novel transcriptional activator, the locus of enterocyte effacement (LEE)-encoded regulator (Ler). Mol Microbiol 1999, 33:296-306.
33. Deng W, Puente JL, Gruenheid S, Li Y, Vallance BA, Vazquez A, Barba J, Ibarra JA, O'Donnell P, Metalnikov P, Ashman K, Lee S, Goode D, Pawson T, Finlay BB: Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci U S A 2004, 101:3597-3602.
34. Park J, Teichmann SA, Hubbard T, Chothia C: Intermediate sequences increase the detection of homology between sequences. J Mol Biol 1997, 273:349-354.
35. Park J, Karplus K, Barrett C, Hughey R, Haussler D, Hubbard T, Chothia C: Sequence comparisons using multiple sequences detect three times as many remote homologues as pairwise methods. J Mol Biol 1998, 284:1201-1210.
36. Muller A, MacCallum RM, Sternberg MJ: Benchmarking PSIBLAST in genome annotation. J Mol Biol 1999, 293:1257-1271.
37. Jones DT, Swindells MB: Getting the most from PSI-BLAST. Trends Biochem Sci 2002, 27:161-164.
38. Stevens FJ, Kuemmel C, Babnigg G, Collart FR: Efficient recognition of protein fold at low sequence identity by conservative application of Psi-BLAST: application. J Mol Recognit 2004.
39. Stevens FJ: Efficient recognition of protein fold at low sequence identity by conservative application of Psi-BLAST: validation. J Mol Recognit 2004.
40. Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, Khanna A, Marshall M, Moxon S, Sonnhammer EL, Studholme DJ, Yeats C, Eddy SR: The Pfam protein families database. Nucleic Acids Res 2004, 32 Database issue:D138-41.
41. Betts HJ, Chaudhuri RR, Pallen MJ: An analysis of type-III secretion gene clusters in Chromobacterium violaceum. Trends Microbiol 2004, 12:476-482.
42. Marches O, Ledger TN, Boury M, Ohara M, Tu X, Goffaux F, Mainil J, Rosenshine I, Sugai M, De Rycke J, Oswald E: Enteropathogenic and enterohaemorrhagic Escherichia coli deliver a novel effector called Cif, which blocks cell cycle G2/M transition. Mol Microbiol 2003, 50:1553-1567.
43. Mundy R, Petrovska L, Smollett K, Simpson N, Wilson RK, Yu J, Tu X, Rosenshine I, Clare S, Dougan G, Frankel G: Identification of a novel Citrobacter rodentium type III secreted protein, EspI, and roles of this and other secreted proteins in infection. Infect Immun 2004, 72:2288-2302.
44. Garmendia J, Phillips AD, Carlier MF, Chong Y, Schuller S, Marches O, Dahan S, Oswald E, Shaw RK, Knutton S, Frankel G: TccP is an enterohaemorrhagic Escherichia coli O157:H7 type III effector protein that couples Tir to the actin-cytoskeleton. Cell Microbiol 2004, 6:1167-1183.
45. Campellone KG, Robbins D, Leong JM: EspFU is a translocated EHEC effector that interacts with Tir and N-WASP and promotes Nck-independent actin assembly. Dev Cell 2004, 7:217-228.
46. Kanack K, Crawford JA, Karmali MA, Kaper JB: SepZ, a Novel Enteropathogenic Escherichia coli Type-III System Secreted and Translocated Protein: Mutation Does Not Delay Secretion of EspA/B or Translocation of Tir. . [abstract] American Society for Microbiology General Meeting, New Orleans 2004.
47. Elliott SJ, Wainwright LA, McDaniel TK, Jarvis KG, Deng YK, Lai LC, McNamara BP, Donnenberg MS, Kaper JB: The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69. Mol Microbiol 1998, 28:1-4.
48. Kresse AU, Schulze K, Deibel C, Ebel F, Rohde M, Chakraborty T, Guzman CA: Pas, a novel protein required for protein secretion and attaching and effacing activities of enterohemorrhagic Escherichia coli. J Bacteriol 1998, 180:4370-4379.
49. Gauthier A, Puente JL, Finlay BB: Secretin of the enteropathogenic Escherichia coli type III secretion system requires components of the type III apparatus for assembly and localization. Infect Immun 2003, 71:3310-3319.
50. Gauthier A, Finlay BB: Translocated intimin receptor and its chaperone interact with ATPase of the type III secretion apparatus of enteropathogenic Escherichia coli. J Bacteriol 2003, 185:6747-6755.
51. Jackson MW, Plano GV: DsbA is required for stable expression of outer membrane protein YscC and for efficient Yop secretion in Yersinia pestis. J Bacteriol 1999, 181:5126-5130.
52. Pallen M, Chaudhuri R, Khan A: Bacterial FHA domains: neglected players in the phospho-threonine signalling game? Trends Microbiol 2002, 10:556-563.
53. Yeats C, Bateman A: The BON domain: a putative membranebinding domain. Trends Biochem Sci 2003, 28:352-355.
54. Jackson MW, Plano GV: Interactions between type III secretion apparatus components from Yersinia pestis detected using the yeast two-hybrid system. FEMS Microbiol Lett 2000, 186:85-90.
55. Marchler-Bauer A, Anderson JB, Cherukuri PF, Deweese-Scott C, Geer LY, Gwadz M, He S, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Liebert CA, Liu C, Lu F, Marchler GH, Mullokandov M, Shoemaker BA, Simonyan V, Song JS, Thiessen PA, Yamashita RA, Yin JJ, Zhang D, Bryant SH: CDD: a Conserved Domain Database for protein classification. Nucleic Acids Res 2005, 33 Database Issue:D192-6.
56. Fadouloglou VE, Tampakaki AP, Glykos NM, Bastaki MN, Hadden JM, Phillips SE, Panopoulos NJ, Kokkinidis M: Structure of HrcQB-C, a conserved component of the bacterial type III secretion systems. Proc Natl Acad Sci U S A 2004, 101:70-75.
57. Minamino T, MacNab RM: FliH, a soluble component of the type III flagellar export apparatus of Salmonella, forms a complex with FliI and inhibits its ATPase activity. Mol Microbiol 2000, 37:1494-1503.
58. Koraimann G: Lytic transglycosylases in macromolecular transport systems of Gram-negative bacteria. Cell Mol Life Sci 2003, 60:2371-2388.
59. Thunnissen AM, Dijkstra AJ, Kalk KH, Rozeboom HJ, Engel H, Keck W, Dijkstra BW: Doughnut-shaped structure of a bacterial muramidase revealed by X-ray crystallography. Nature 1994, 367:750-753.
60. Thunnissen AM, Rozeboom HJ, Kalk KH, Dijkstra BW: Structure of the 70-kDa soluble lytic transglycosylase complexed with bulgecin A. Implications for the enzymatic mechanism. Biochemistry 1995, 34:12729-12737.
61. van Asselt EJ, Kalk KH, Dijkstra BW: Crystallographic studies of the interactions of Escherichia coli lytic transglycosylase Slt35 with peptidoglycan. Biochemistry 2000, 39:1924-1934.
62. Wilson RK, Shaw RK, Daniell S, Knutton S, Frankel G: Role of EscF, a putative needle complex protein, in the type III protein translocation system of enteropathogenic Escherichia coli. Cell Microbiol 2001, 3:753-762.
63. Sekiya K, Ohishi M, Ogino T, Tamano K, Sasakawa C, Abe A: Supermolecular structure of the enteropathogenic Escherichia coli type III secretion system and its direct interaction with the EspA-sheath-like structure. Proc Natl Acad Sci U S A 2001, 98:11638-11643.
64. Hoiczyk E, Blobel G: Polymerization of a single protein of the pathogen Yersinia enterocolitica into needles punctures eukaryotic cells. Proc Natl Acad Sci U S A 2001, 98:4669-4674.
65. Sukhan A, Kubori T, Galan JE: Synthesis and localization of the Salmonella SPI-1 type III secretion needle complex proteins PrgI and PrgJ. J Bacteriol 2003, 185:3480-3483.
66. Kimbrough TG, Miller SI: Contribution of Salmonella typhimurium type III secretion components to needle complex formation. Proc Natl Acad Sci U S A 2000, 97:11008-11013.
67. Kubori T, Sukhan A, Aizawa SI, Galan JE: Molecular characterization and assembly of the needle complex of the Salmonella typhimurium type III protein secretion system. Proc Natl Acad Sci U S A 2000, 97:10225-10230.
68. Tamano K, Aizawa S, Katayama E, Nonaka T, Imajoh-Ohmi S, Kuwae A, Nagai S, Sasakawa C: Supramolecular structure of the Shigella type III secretion machinery: the needle part is changeable in length and essential for delivery of effectors. Embo J 2000, 19:3876-3887.
69. Blocker A, Jouihri N, Larquet E, Gounon P, Ebel F, Parsot C, Sansonetti P, Allaoui A: Structure and composition of the Shigella flexneri "needle complex", a part of its type III secreton. Mol Microbiol 2001, 39:652-663.
70. Marlovits TC, Kubori T, Sukhan A, Thomas DR, Galan JE, Unger VM: Structural insights into the assembly of the type III secretion needle complex. Science 2004, 306:1040-1042.
71. Ebel F, Podzadel T, Rohde M, Kresse AU, Kramer S, Deibel C, Guzman CA, Chakraborty T: Initial binding of Shiga toxin-producing Escherichia coli to host cells and subsequent induction of actin rearrangements depend on filamentous EspA-containing surface appendages. Mol Microbiol 1998, 30:147-161.
72. Knutton S, Rosenshine I, Pallen MJ, Nisan I, Neves BC, Bain C, Wolff C, Dougan G, Frankel G: A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. Embo J 1998, 17:2166-2176.
73. Daniell SJ, Kocsis E, Morris E, Knutton S, Booy FP, Frankel G: 3D structure of EspA filaments from enteropathogenic Escherichia coli. Mol Microbiol 2003, 49:301-308.
74. Ide T, Laarmann S, Greune L, Schillers H, Oberleithner H, Schmidt MA: Characterization of translocation pores inserted into plasma membranes by type III-secreted Esp proteins of enteropathogenic Escherichia coli. Cell Microbiol 2001, 3:669-679.
75. Samatey FA, Imada K, Nagashima S, Vonderviszt F, Kumasaka T, Yamamoto M, Namba K: Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature 2001, 410:331-337.
76. Yonekura K, Maki-Yonekura S, Namba K: Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 2003, 424:643-650.
77. Mimori-Kiyosue Y, Vonderviszt F, Yamashita I, Fujiyoshi Y, Namba K: Direct interaction of flagellin termini essential for polymorphic ability of flagellar filament. Proc Natl Acad Sci U S A 1996, 93:15108-15113.
78. Yoshioka K, Aizawa S, Yamaguchi S: Flagellar filament structure and cell motility of Salmonella typhimurium mutants lacking part of the outer domain of flagellin. J Bacteriol 1995, 177:1090-1093.
79. Macnab RM: Flagella and motility. In Escherichia coli and Salmonella: Cellular and Molecular Biology Edited by: Neidhardt FC, Curtiss III R, Ingraham JL, Lin ECC, Low KB, et al. Washington, DC: ASM Press; 1996:123-145.
80. Homma M, DeRosier DJ, Macnab RM: Flagellar hook and hookassociated proteins of Salmonella typhimurium and their relationship to other axial components of the flagellum. J Mol Biol 1990, 213:819-832.
81. Pallen MJ, Dougan G, Frankel G: Coiled-coil domains in proteins secreted by type III secretion systems. Mol Microbiol 1997, 25:423-425.
82. Delahay RM, Knutton S, Shaw RK, Hartland EL, Pallen MJ, Frankel G: The coiled-coil domain of EspA is essential for the assembly of the type III secretion translocon on the surface of enteropathogenic Escherichia coli. J Biol Chem 1999, 274:35969-35974.
83. Yip CK, Finlay BB, Strynadka NC: Structural characterization of a type III secretion system filament protein in complex with its chaperone. Nat Struct Mol Biol 2005, 12:75-81.
84. Smith KD, Andersen-Nissen E, Hayashi F, Strobe K, Bergman MA, Barrett SL, Cookson BT, Aderem A: Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat Immunol 2003, 4:1247-1253.
85. Delahay RM, Frankel G: Coiled-coil proteins associated with type III secretion systems: a versatile domain revisited. Mol Microbiol 2002, 45:905-916.
86. Kresse AU, Beltrametti F, Muller A, Ebel F, Guzman CA: Characterization of SepL of enterohemorrhagic Escherichia coli. J Bacteriol 2000, 182:6490-6498.
87. O'Connell CB, Creasey EA, Knutton S, Elliott S, Crowther LJ, Luo W, Albert MJ, Kaper JB, Frankel G, Donnenberg MS: SepL, a protein required for enteropathogenic Escherichia coli type III translocation, interacts with secretion component SepD. Mol Microbiol 2004, 52:1613-1625.
88. Marcotte EM, Pellegrini M, Thompson MJ, Yeates TO, Eisenberg D: A combined algorithm for genome-wide prediction of protein function. Nature 1999, 402:83-86.
89. Enright AJ, Ouzounis CA: Functional associations of proteins in entire genomes by means of exhaustive detection of gene fusions. Genome Biol 2001, 2:RESEARCH0034.
90. Enright AJ, Iliopoulos I, Kyrpides NC, Ouzounis CA: Protein interaction maps for complete genomes based on gene fusion events. Nature 1999, 402:86-90.
91. Ferracci F, Day JB, Ezelle HJ, Plano GV: Expression of a functional secreted YopN-TyeA hybrid protein in Yersinia pestis is the result of a +1 translational frameshift event. J Bacteriol 2004, 186:5160-5166.
92. Fields KA, Hackstadt T: Evidence for the secretion of Chlamydia trachomatis CopN by a type III secretion mechanism. Mol Microbiol 2000, 38:1048-1060.
93. Sundberg L, Forsberg A: TyeA of Yersinia pseudotuberculosis is involved in regulation of Yop expression and is required for polarized translocation of Yop effectors. Cell Microbiol 2003, 5:187-202.
94. Marenne MN, Journet L, Mota LJ, Cornelis GR: Genetic analysis of the formation of the Ysc-Yop translocation pore in macrophages by Yersinia enterocolitica: role of LcrV, YscF and YopN. Microb Pathog 2003, 35:243-258.
95. Cheng LW, Kay O, Schneewind O: Regulated secretion of YopN by the type III machinery of Yersinia enterocolitica. J Bacteriol 2001, 183:5293-5301.
96. Cheng LW, Schneewind O: Yersinia enterocolitica TyeA, an intracellular regulator of the type III machinery, is required for specific targeting of YopE, YopH, YopM, and YopN into the cytosol of eukaryotic cells. J Bacteriol 2000, 182:3183-3190.
97. Iriarte M, Sory MP, Boland A, Boyd AP, Mills SD, Lambermont I, Cornelis GR: TyeA, a protein involved in control of Yop release and in translocation of Yersinia Yop effectors. Embo J 1998, 17:1907-1918.
98. Kubori T, Galan JE: Salmonella type III secretion-associated protein InvE controls translocation of effector proteins into host cells. J Bacteriol 2002, 184:4699-4708.
99. Matson JS, Nilles ML: LcrG-LcrV interaction is required for control of Yops secretion in Yersinia pestis. J Bacteriol 2001, 183:5082-5091.
100. DeBord KL, Lee VT, Schneewind O: Roles of LcrG and LcrV during type III targeting of effector Yops by Yersinia enterocolitica. J Bacteriol 2001, 183:4588-4598.
101. Journet L, Agrain C, Broz P, Cornelis GR: The needle length of bacterial injectisomes is determined by a molecular ruler. Science 2003, 302:1757-1760.
102. Minamino T, Gonzalez-Pedrajo B, Yamaguchi K, Aizawa SI, Macnab RM: FliK, the protein responsible for flagellar hook length control in Salmonella, is exported during hook assembly. Mol Microbiol 1999, 34:295-304.
103. Makishima S, Komoriya K, Yamaguchi S, Aizawa SI: Length of the flagellar hook and the capacity of the type III export apparatus. Science 2001, 291:2411-2413.
104. Magdalena J, Hachani A, Chamekh M, Jouihri N, Gounon P, Blocker A, Allaoui A: Spa32 regulates a switch in substrate specificity of the type III secreton of Shigella flexneri from needle components to Ipa proteins. J Bacteriol 2002, 184:3433-3441.
105. Geourjon C, Deleage G: SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. Comput Appl Biosci 1995, 11:681-684.
106. Wainwright LA, Kaper JB: EspB and EspD require a specific chaperone for proper secretion from enteropathogenic Escherichia coli. Mol Microbiol 1998, 27:1247-1260.
107. Abe A, de Grado M, Pfuetzner RA, Sanchez-Sanmartin C, Devinney R, Puente JL, Strynadka NC, Finlay BB: Enteropathogenic Escherichia coli translocated intimin receptor, Tir, requires a specific chaperone for stable secretion. Mol Microbiol 1999, 33:1162-1175.
108. Elliott SJ, Hutcheson SW, Dubois MS, Mellies JL, Wainwright LA, Batchelor M, Frankel G, Knutton S, Kaper JB: Identification of CesT, a chaperone for the type III secretion of Tir in enteropathogenic Escherichia coli. Mol Microbiol 1999, 33:1176-1189.
109. Luo Y, Bertero MG, Frey EA, Pfuetzner RA, Wenk MR, Creagh L, Marcus SL, Lim D, Sicheri F, Kay C, Haynes C, Finlay BB, Strynadka NC: Structural and biochemical characterization of the type III secretion chaperones CesT and SigE. Nat Struct Biol 2001, 8:1031-1036.
110. Evdokimov AG, Tropea JE, Routzahn KM, Waugh DS: Threedimensional structure of the type III secretion chaperone SycE from Yersinia pestis. Acta Crystallogr D Biol Crystallogr 2002, 58:398-406.
111. Stebbins CE, Galan JE: Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 2001, 414:77-81.
112. van Eerde A, Hamiaux C, Perez J, Parsot C, Dijkstra BW: Structure of Spa15, a type III secretion chaperone from Shigella flexneri with broad specificity. EMBO Rep 2004, 5:477-483.
113. Frank DW, Iglewski BH: Cloning and sequence analysis of a trans-regulatory locus required for exoenzyme S synthesis in Pseudomonas aeruginosa. J Bacteriol 1991, 173:6460-6468.
114. Dasgupta N, Lykken GL, Wolfgang MC, Yahr TL: A novel anti-antiactivator mechanism regulates expression of the Pseu-domonas aeruginosa type III secretion system. Mol Microbiol 2004, 53:297-308.
115. Pallen MJ, Francis MS, Futterer K: Tetratricopeptide-like repeats in type-III-secretion chaperones and regulators. FEMS Microbiol Lett 2003, 223:53-60.
116. Barve SS, Straley SC: lcrR, a low-Ca2(+)-response locus with dual Ca2(+)-dependent functions in Yersinia pestis. J Bacteriol 1990, 172:4661-4671.
117. Skryzpek E, Straley SC: LcrG, a secreted protein involved in negative regulation of the low-calcium response in Yersinia pestis. J Bacteriol 1993, 175:3520-3528.
118. Mecsas J, Bilis I, Falkow S: Identification of attenuated Yersinia pseudotuberculosis strains and characterization of an orogastric infection in BALB/c mice on day 5 postinfection by signature-tagged mutagenesis. Infect Immun 2001, 69:2779-2787.
119. Bolin I, Portnoy DA, Wolf-Watz H: Expression of the temperature-inducible outer membrane proteins of yersiniae. Infect Immun 1985, 48:234-240.
120. Elliott SJ, Sperandio V, Giron JA, Shin S, Mellies JL, Wainwright L, Hutcheson SW, McDaniel TK, Kaper JB: The locus of enterocyte effacement (LEE)-encoded regulator controls expression of both LEE- and non-LEE-encoded virulence factors in enteropathogenic and enterohemorrhagic Escherichia coli. Infect Immun 2000, 68:6115-6126.
121. Haack KR, Robinson CL, Miller KJ, Fowlkes JW, Mellies JL: Interaction of Ler at the LEE5 (tir) operon of enteropathogenic Escherichia coli. Infect Immun 2003, 71:384-392.
122. Sperandio V, Mellies JL, Delahay RM, Frankel G, Crawford JA, Nguyen W, Kaper JB: Activation of enteropathogenic Escherichia coli (EPEC) LEE2 and LEE3 operons by Ler. Mol Microbiol 2000, 38:781-793.
123. Bustamante VH, Santana FJ, Calva E, Puente JL: Transcriptional regulation of type III secretion genes in enteropathogenic Escherichia coli: Ler antagonizes H-NS-dependent repression. Mol Microbiol 2001, 39:664-678.
124. Dorman CJ, Hinton JC, Free A: Domain organization and oligomerization among H-NS-like nucleoid-associated proteins in bacteria. Trends Microbiol 1999, 7:124-128.
125. Rimsky S: Structure of the histone-like protein H-NS and its role in regulation and genome superstructure. Curr Opin Microbiol 2004, 7:109-114.
126. Tendeng C, Bertin PN: H-NS in Gram-negative bacteria: a family of multifaceted proteins. Trends Microbiol 2003, 11:511-518.
127. Beloin C, Deighan P, Doyle M, Dorman CJ: Shigella flexneri 2a strain 2457T expresses three members of the H-NS-like protein family: characterization of the Sfh protein. Mol Genet Genomics 2003, 270:66-77.
128. Deighan P, Beloin C, Dorman CJ: Three-way interactions among the Sfh, StpA and H-NS nucleoid-structuring proteins of Shigella flexneri 2a strain 2457T. Mol Microbiol 2003, 48:1401-1416.
129. Paytubi S, Madrid C, Forns N, Nieto JM, Balsalobre C, Uhlin BE, Juarez A: YdgT, the Hha paralogue in Escherichia coli, forms heteromeric complexes with H-NS and StpA. Mol Microbiol 2004, 54:251-263.
130. Sperandio V, Mellies JL, Nguyen W, Shin S, Kaper JB: Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proc Natl Acad Sci U S A 1999, 96:15196-15201.
131. Sperandio V, Torres AG, Giron JA, Kaper JB: Quorum sensing is a global regulatory mechanism in enterohemorrhagic Escherichia coli O157:H7. J Bacteriol 2001, 183:5187-5197.
132. Sperandio V, Li CC, Kaper JB: Quorum-sensing Escherichia coli regulator A: a regulator of the LysR family involved in the regulation of the locus of enterocyte effacement pathogenicity island in enterohemorrhagic E. coli. Infect Immun 2002, 70:3085-3093.
133. Sperandio V, Torres AG, Kaper JB: Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli. Mol Microbiol 2002, 43:809-821.
134. Sperandio V, Torres AG, Jarvis B, Nataro JP, Kaper JB: Bacteriahost communication: the language of hormones. Proc Natl Acad Sci U S A 2003, 100:8951-8956.
135. Kanamaru K, Tatsuno I, Tobe T, Sasakawa C: SdiA, an Escherichia coli homologue of quorum-sensing regulators, controls the expression of virulence factors in enterohaemorrhagic Escherichia coli O157:H7. Mol Microbiol 2000, 38:805-816.
136. Ahmer BM: Cell-to-cell signalling in Escherichia coli and Salmonella enterica. Mol Microbiol 2004, 52:933-945.
137. Ahmer BM, van Reeuwijk J, Timmers CD, Valentine PJ, Heffron F: Salmonella typhimurium encodes an SdiA homolog, a putative quorum sensor of the LuxR family, that regulates genes on the virulence plasmid. J Bacteriol 1998, 180:1185-1193.
138. Michael B, Smith JN, Swift S, Heffron F, Ahmer BM: SdiA of Salmonella enterica is a LuxR homolog that detects mixed microbial communities. J Bacteriol 2001, 183:5733-5742.
139. Volf J, Sevcik M, Havlickova H, Sisak F, Damborsky J, Rychlik I: Role of SdiA in Salmonella enterica serovar Typhimurium physiology and virulence. Arch Microbiol 2002, 178:94-101.
140. Smith JN, Ahmer BM: Detection of other microbial species by Salmonella: expression of the SdiA regulon. J Bacteriol 2003, 185:1357-1366.
141. Henke JM, Bassler BL: Quorum sensing regulates type III secretion in Vibrio harveyi and Vibrio parahaemolyticus. J Bacteriol 2004, 186:3794-3805.
142. Slack FJ, Ruvkun G: A novel repeat domain that is often associated with RING finger and B-box motifs. Trends Biochem Sci 1998, 23:474-475.
143. Edwards TA, Wilkinson BD, Wharton RP, Aggarwal AK: Model of the brain tumor-Pumilio translation repressor complex. Genes Dev 2003, 17:2508-2513.
144. Lio JC, Syu WJ: Identification of a negative regulator for the pathogenicity island of enterohemorrhagic Escherichia coli O157:H7. J Biomed Sci 2004, 11:855-863.
145. Creasey EA, Delahay RM, Daniell SJ, Frankel G: Yeast two-hybrid system survey of interactions between LEE-encoded proteins of enteropathogenic Escherichia coli. Microbiology 2003, 149:2093-2106.
146. Janakiraman A, Slauch JM: The putative iron transport system SitABCD encoded on SPI1 is required for full virulence of Salmonella typhimurium. Mol Microbiol 2000, 35:1146-1155.
147. Allaoui A, Schulte R, Cornelis GR: Mutational analysis of the Yersinia enterocolitica virC operon: characterization of yscE, F, G, I, J, K required for Yop secretion and yscH encoding YopR. Mol Microbiol 1995, 18:343-355.
148. Swietnicki W, O'Brien S, Holman K, Cherry S, Brueggemann E, Tropea JE, Hines HB, Waugh DS, Ulrich RG: Novel protein-protein interactions of the Yersinia pestis type III secretion system elucidated with a matrix analysis by surface plasmon resonance and mass spectrometry. J Biol Chem 2004, 279:38693-38700.
149. Day JB, Guller I, Plano GV: Yersinia pestis YscG protein is a Syclike chaperone that directly binds yscE. Infect Immun 2000, 68:6466-6471.
150. Yu XJ, Liu M, Holden DW: SsaM and SpiC interact and regulate secretion of Salmonella Pathogenicity Island 2 type III secretion system effectors and translocators. Mol Microbiol 2004, 54:604-619.
151. Hmmer [http://hmmer.wustl.edu/]
152. Letunic I, Copley RR, Schmidt S, Ciccarelli FD, Doerks T, Schultz J, Ponting CP, Bork P: SMART 4.0: towards genomic data integration. Nucleic Acids Res 2004, 32 Database issue:D142-4.
153. Notredame C, Higgins DG, Heringa J: T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 2000, 302:205-217.
154. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD: Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 2003, 31:3497-3500.
155. Goodstadt L, Ponting CP: CHROMA: consensus-based colouring of multiple alignments for publication. Bioinformatics 2001, 17:845-846.
156. Burghout P, van Boxtel R, Van Gelder P, Ringler P, Muller SA, Tommassen J, Koster M: Structure and electrophysiological properties of the YscC secretin from the type III secretion system of Yersinia enterocolitica. J Bacteriol 2004, 186:4645-4654.
157. Cornelis GR: The Yersinia Ysc-Yop 'type III' weaponry. Nat Rev Mol Cell Biol 2002, 3:742-752.
158. Van Arnam JS, McMurry JL, Kihara M, Macnab RM: Analysis of an engineered Salmonella flagellar fusion protein, FliR-FlhB. J Bacteriol 2004, 186:2495-2498.
159. Lavander M, Sundberg L, Edqvist PJ, Lloyd SA, Wolf-Watz H, Forsberg A: Proteolytic cleavage of the FlhB homologue YscU of Yersinia pseudotuberculosis is essential for bacterial survival but not for type III secretion. J Bacteriol 2002, 184:4500-4509.
160. Edqvist PJ, Olsson J, Lavander M, Sundberg L, Forsberg A, Wolf-Watz H, Lloyd SA: YscP and YscU regulate substrate specificity of the Yersinia type III secretion system. J Bacteriol 2003, 185:2259-2266.
161. Pucciarelli MG, Garcia-del Portillo F: Protein-peptidoglycan interactions modulate the assembly of the needle complex in the Salmonella invasion-associated type III secretion system. Mol Microbiol 2003, 48:573-585.
162. Suzuki H, Yonekura K, Namba K: Structure of the rotor of the bacterial flagellar motor revealed by electron cryomicroscopy and single-particle image analysis. J Mol Biol 2004, 337:105-113.
163. Suzuki H, Yonekura K, Murata K, Hirai T, Oosawa K, Namba K: A structural feature in the central channel of the bacterial flagellar FliF ring complex is implicated in type III protein export. J Struct Biol 1998, 124:104-114.
164. Carrillo CD, Taboada E, Nash JH, Lanthier P, Kelly J, Lau PC, Verhulp R, Mykytczuk O, Sy J, Findlay WA, Amoako K, Gomis S, Willson P, Austin JW, Potter A, Babiuk L, Allan B, Szymanski CM: Genomewide expression analyses of
165. Niehus E, Gressmann H, Ye F, Schlapbach R, Dehio M, Dehio C, Stack A, Meyer TF, Suerbaum S, Josenhans C: Genome-wide analysis of transcriptional hierarchy and feedback regulation in the flagellar system of Helicobacter pylori. Mol Microbiol 2004, 52:947-961.